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Keywords:

  • duodenum;
  • gastrointestinal motility;
  • manometry;
  • peristalsis

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

MMC-related retroperistalsis is a cyclical phenomenon in the duodenum linked to phase III. The aim of this study was to elucidate the direction of propagation of juxtapyloric duodenal pressure waves in the postprandial state in healthy humans and to compare with the contractions in the interdigestive phase II. Antroduodenal manometry was performed in 11 healthy subjects. Individual pressure waves propagating along a 6-cm duodenal segment were analysed with respect to the proportions of antegrade and retrograde propagation in the four duodenal subsegments (D1–D2) to (D4–D5), each subsegment being 15 mm. A test meal was given 30 min after a phase III had passed and motility recording continued for 60 min after the meal. During both the first and the second 30-min period of postprandial recording the proportion of retrograde pressure waves was larger just distal to the pylorus, (D1–D2), 40% (23–68) and 50% (23–68), respectively, compared to the distal part, (D4–D5), of the duodenal segment, 29% (12–30) and 10%(10–24), respectively (P < 0.05 and 0.01). In contrast, during late phase II of the interdigestive state antegrade pressure waves predominated in all four duodenal subsegments. We conclude that in the postprandial state a high proportion of the duodenal pressure waves (40–50%) is retrograde in the immediate juxtapyloric area while antegrade contractions predominate at a distance 5–6 cm distal to the pylorus. These manometric data together with recent observations of postprandial transpyloric liquid flow, indicate that retrograde duodenogastric propelling of contents may be an important determinant for the gastric emptying rate.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

The peristaltic activity of the duodenum is the main determinant of intraluminal duodenal, aborad and orad transport. Gastric emptying may also be influenced by duodenal contractility, particularly by the activity in the most proximal parts.1–4 However, few manometric studies have been devoted to detailed analysis of duodenal peristalsis in the postprandial situation in humans. Direct studies of duodenal propagation patterns have given conflicting results. In one study on fasting and fed motility only antegrade contractions were reported.5 According to Kerrigan et al.6 most postprandial pressure waves in the proximal duodenum are antegrade in healthy subjects, only a minority being retrograde.

Recently, duodenal manometry with high temporal and spatial resolution showed that retroperistalsis is a prominent feature of the last part of phase III of the migrating motor complex (MMC) in the descendent part of the duodenum.7 Moreover, in the juxtapyloric duodenal area, retrograde pressure waves predominate even in the early part of phase III which coincides with late antral phase III. This means that antral and juxtapyloric duodenal contractions are on a collision course.8

The exact function of the phase III related duodenal retroperistalsis is unknown, but regulation of the interdigestive gastric emptying may be a possible function although direct studies have not been performed.

These observations give rise to the question of whether duodenal retroperistalsis could be of importance in the postprandial situation. In the descendent duodenum, near the papilla, retrograde propagation of pressure waves was infrequent postprandially.7 However, the direction of propagation of individual postprandial contractions in the juxtapyloric area has not been investigated in detail with a high resolution technique. Another interesting issue is whether the postprandial duodenal pressure waves differ spatially from those of phase II of the MMC, despite the temporal similarities in the two situations.

The aim of this study was to characterize the direction of propagation of juxtapyloric duodenal pressure waves in the postprandial state in healthy humans and to compare with the activity in the interdigestive phase II of the MMC.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

Eleven healthy subjects (six women and five men) with a mean age of 29 years (range 21–37 years) were studied. They had no history of gastrointestinal or chronic disease and none of the subjects were taking any medication on a regular basis. They were all within normal range of body weight. The study was approved by the Ethical Committee of the University of Göteborg.

Experimental design

Gastroduodenal motility was recorded after an overnight fast. The subjects were in a semi-reclined position during registration. A multi-channel catheter with pressure recording points 15 mm apart was used. Adjacent side-ports had a radial separation of 90° or 135°. The catheter had an outer diameter of 4.8 mm, a central lumen of 1.8 mm for the guide wire, and eight lumens for manometry, each having a diameter of 0.8 mm. These channels were connected to capillaries and each channel was perfused with water at a rate of 0.3 mL min−1. The catheter was connected to pressure transducers and recordings were made by a PC polygraph (Synectics Medical, Stockholm, Sweden), which converted the pressure data to digital information at 4 Hz. The information was transferred to an IBM compatible computer via a fibre-optic interface. The individual registrations were displayed on the computer screen during the recording and stored for later analysis (Synectics Polygram, Version 5.06 × 1). The catheter was placed under fluoroscopic guidance so that two or three recording points seemed to be in the antrum and five or six recording points in the proximal duodenum, just distal to the pylorus. Appropriate adjustments were then performed at the beginning of the recording session when the typical antroduodenal pressure waves appeared on the screen. The intention was that at least five side-ports, i.e. a 6-cm segment, had a duodenal motor pattern. Appropriate criteria for localization of the pylorus in the recording were applied.9 The most proximal recording point yielding a duodenal profile was denoted D1, and the following recording points situated 15 mm apart, D2–D5. The side-ports divided the 6-cm segment into four duodenal subsegments, (D1–D2) to (D4–D5), each subsegment being 1.5 cm. A test meal was given 30 min after a phase III had passed and motility recording continued for 60 min after the meal. The standardized meal consisted of porridge (made from 50 g rolled oats, 200 mL of water), 150 mL of milk, white bread (50 g), butter (10 g) and about 13 g of cheese (16% fat). The total energy content was 500 kCal. Just prior to the meal the catheter was advanced 3–5 cm to compensate for the gastric accommodation response.

Analysis

The interdigestive propagated pressure waves were analysed for late phase II (at least 10 propagated pressure waves during the last 30 min) with respect to the proportion of antegrade and retrograde propagation. The postprandial pressure waves were calculated for two 30-min periods (at least 10 propagated pressure waves in each period) and analysed in the same respect as the pressure waves in late phase II. The first 30-min period was likely to include emptying of liquids and the lag phase for solids, and the second period to include emptying of solids. Pressure waves should have amplitudes ≥ 10 mmHg to be included. The propagated pressure waves were visually recognized and manually marked applying an upper limit of 4.75 sec of the time window chosen for a 4.5-cm segment. This corresponds to the previously applied time window for a 4.0-cm segment.7 After that the migration velocity of individual pressure waves was calculated by the computer program as propagation of the peaks of the pressure waves for the 1.5-cm subsegments. The lower limit of the time window chosen for each 1.5-cm subsegment was 0.25 sec, determined by the discrimination power of the digital 4 Hz recording. This lower limit allowed calculation for individual pressure waves with a velocity up to 6 cm sec−1. A positive velocity value indicated antegrade waves, and a negative velocity value indicated retrograde waves. Pressure waves with higher velocities were classified and included in the statistics as stationary or simultaneous for that subsegment.

Another criterion for inclusion was that each pressure wave should be followed along the whole 6-cm segment between recording points D1 and D5.

Statistical analysis

The proportions of antegrade and retrograde pressure waves are expressed as medians and interquartile range (IQR). ANOVA was used for the statistical comparisons.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

Original recordings of postprandial duodenal pressure waves in the juxtapyloric area are shown with high time resolution in Figs 1 and 2. D1–D5 correspond to the five duodenal recording points. The figures demonstrate examples of retrograde and antegrade pressure waves. In Fig. 1 the origin of the propagated pressure wave seems to be at the D2 level. From this level the pressure wave diverges in an antegrade direction distally in the duodenum and in a retrograde fashion to the most proximal part of the duodenum. The retrograde character is evident from the propagation of the peak of the pressure wave, and also from the onset of the pressure wave. In Fig. 2 another diverging duodenal pressure wave is shown but this time during antral quiescence. Figure 2 also shows a strictly antegrade pressure event recorded while the antrum was inactive.

image

Figure 1. Example of a postprandial divergent duodenal pressure wave appearing simultaneously with antral activity (two top tracings). The duodenal wave starts at recording point D2 and migrates in the orad and aborad directions. Pressure recording performed in eight recording points with 15 mm interval and with very high time resolution.

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image

Figure 2. Two examples of postprandial duodenal pressure waves appearing during a minute with low activity in the distal antrum (top tracing). One pressure wave, starting in D2, is diverging (cf. Fig. 1) while one is purely antegrade from level D1 to D5.

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Phase II

During late phase II (last 30 min) of the interdigestive state antegrade pressure waves predominated in all four duodenal subsegments, (D1–D2) to (D4–D5) (Fig. 3 and Table 1). Out of all pressure waves in phase II 60–80% (medians) were antegrade and 10% were retrograde. According to our criteria 10–30% were simultaneous within the subsegments.

Table 1.  The proportion (%) of retrograde and antegrade pressure waves out of all pressure waves presented as medians and interquartile range (IQR) for phase 2 and the two postprandial periods in the four duodenal subsegments (D1–D2) to (D4–D5). Thumbnail image of
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Figure 3. Prevalence of antegrade, retrograde and simultaneous pressure waves (medians) in the four consecutive subsegments in the proximal duodenum. Early and late postprandial periods (PP) correspond to 0–30 and 30–60 min, respectively, after the meal. Note the predominance of antegrade contractions in phase II and the high postprandial frequency of retrograde pressure waves in the most juxtapyloric subsegment.

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Postprandial conditions

Figure 3 illustrates the proportion (medians) of antegrade, retrograde and simultaneous pressure waves in all four duodenal subsegments, (D1–D2) to (D4–D5), in the interdigestive late phase II and the early and late postprandial period. In contrast to phase II the postprandial periods showed a high median proportion (40–50%) of retrograde pressure waves just distal to the pylorus (D1–D2) (Table 1). Also in the next subsegment (D2–D3) retrograde pressure waves were frequent (30–40%). More distally, in (D3–D4) and (D4–D5), the direction of propagation of pressure waves was mainly antegrade (60–80% and 60–70%, respectively). Thus, the origin of pressure waves in the postprandial state was often some 2–4 cm distal to the pylorus. From this level the pressure waves diverged in proximal and distal directions.

Detailed statistical comparisons were made between the time periods studied and between the proximal and distal duodenal subsegments. In the most proximal part of the duodenum (D1–D2), the proportion of retrograde pressure waves during the first 30 min of postprandial recording was larger (40%) than in the distal end (D4–D5) of the duodenal segment (29%) (< 0.05) (Fig. 4). Also during the last 30 min of postprandial recording retrograde pressure waves were more frequent just distal to the pylorus (D1–D2) (50%) than further distally (D4–D5) (10%) (< 0.01). In late phase II of the interdigestive state there were significantly less retrograde pressure waves in the most proximal subsegment (10%) compared to the two postprandial periods (< 0.01). At the distal end of the 6-cm segment phase II showed less retrograde pressure waves (10%) than during the early postprandial period (< 0.05), but between phase II and the second postprandial period (including emptying of solids) there was no significant difference.

image

Figure 4. Proportions of retrograde pressure waves in the most proximal (D1–D2) and the distal duodenal subsegment (D4–D5) during late phase II and postprandially; 0–30 min (early) and 30–60 min (late) after the test meal. Medians, interquartile ranges and percentiles 10 and 90 are indicated. Postprandial periods are compared with phase II in the same subsegment. *< 0.05 and **< 0.01.

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Calculation of propagation of pressure waves, when using the onsets of pressure waves, yielded very similar results as calculation of the peaks of the pressure waves. In the most proximal duodenal subsegment (D1–D2) there were 1% more retrograde pressure waves during the whole postprandial hour, when using the onsets of the pressure waves instead of the peaks of the pressure waves. In the most distal duodenal subsegment (D4–D5) there were 4% less retrograde pressure waves when using this principal.

In the most proximal part of the duodenum (D1–D2), the median proportion of antegrade pressure waves was smaller during the first half of the postprandial hour (30%) (Table 1), than in the most distal end (D4–D5) (60%) (< 0.01). The proportions of antegrade pressure waves were similar in the second part of the postprandial hour at the proximal (30%) and the distal ends (70%) (< 0.05) of the segment studied. Just distal to the pylorus there was a significantly larger proportion of antegrade pressure waves in late phase II (60%) compared to the two postprandial periods (30%) (< 0.01 and < 0.05, respectively). In the fourth duo-denal subsegment (D4–D5) there was a high proportion of antegrade pressure waves in both late phase II and the whole postprandial hour (80%, 60% and 70%, respectively).

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

The main aim of this study in healthy volunteers was to investigate whether a duodenal retroperistalsis similar to that in the interdigestive phase III8 exists also under postprandial conditions. Furthermore, we wanted to compare the propagation pattern of individual pressure waves in the interdigestive phase II and postprandially as these states, both having irregular frequency of contractions, resemble each other manometrically when using conventional time resolution of the recording.

The present study showed that retroperistalsis in the proximal duodenum is common also in the postprandial state. A high proportion of the pressure waves in both the early (first 30 min) and the late (last 30 min) postprandial hour seemed to start some 2–4 cm distal to the pylorus, and from this level the pressure waves propagated both in an antegrade fashion distally in the duodenum and in a retrograde direction towards the stomach. The appearance of these frequently occurring divergent contractions in the juxtapyloric area resembles the recent findings,8 where divergent contractions and a retroperistaltic sequence were prominent features in early phase III in the interdigestive state. An interesting observation is that the origin of pressure waves occurred at the same level some 2–4 cm distal to the pylorus (corresponding to recording points D2–D3) in both early phase III and in the postprandial periods. The first postprandial 30-min period was likely to include emptying of liquids and the lag phase for solids, while the second postprandial period should include emptying of solids in most subjects. As the proportion of retrograde pressure waves just distal to pylorus was similar in both postprandial periods a specific coupling between retroperistalsis and the lag phase is unlikely.

An important question is whether the juxtapyloric duodenal pressure waves have a real retrotransport function. The retrograde character was evident when analysis was based on the peak as well as on the onset of the pressure waves. This circumstance argues in favour of a real retrograde movement and not a closed chamber phenomenon. Furthermore, before the present study, we observed in two pilot experiments a very close correlation in time between the recording appearance of retrograde pressures and retrograde transport from the duodenum to the antrum of an infused duodenal tracer (111 In-DTPA) assessed by dynamic scintigraphy by gamma camera. Moreover, recent preliminary reported isotope experiments10 have shown a very close correlation between retrograde duodenal pressure waves, recorded with high temporospatial resolution, and the reflux of duodenal contents to the gastric antrum. Thus, the retrograde pressure pattern seems to have a real retropropulsive transport function. Recent electrical recordings of duodenal slow waves in the cat support the existence of such orad duodenal pressure patterns.11

An interesting question is whether the juxtapyloric duodenal retroperistalsis could be involved in regulation of emptying of liquids from the stomach. Emptying of liquids is likely to occur during the whole postprandial hour, initially the ingested liquid and later on the liquidized solids. Our observation of a frequent retroperistalsis just distal to the pylorus is compatible with recent observations by Hausken et al.12 who studied transpyloric flow after a soup meal by a duplex sonographic technique. A duodenogastric reflux was observed in conjunction with 70% of the contractions that involved both the antrum and the duodenum. Most contractions in the duodenal bulb preceded pyloric closure and were often accompanied by a short burst of duodenogastric reflux (cf. Figs 1 and 2). Furthermore, recent studies of postprandial antropyloric flow with the MR-technique by the Nottingham group13 showed nutrient-dependent backflow movements in the distal antrum. Thus, there is support from flow studies that the juxtapyloric postprandial retrograde contractions have a mechanical function leading to retrograde flow involved in the regulation of gastric emptying.

Also other experimental studies indicate that gastric emptying may be influenced by a duodenal break.2,14 Lin et al.2 confirmed that slowing of gastric emptying by hyperosmolar solutions involves a mechanism likely to be increased duodenal resistance. Furthermore, Ehrlein and coworkers1 provided strong evidence that it is not the increase in duodenal motor activity per se, but rather the type of motor pattern which influences gastric emptying. However, the catheters used in these studies did not allow thorough spatial analysis of individual contractions, but the importance of a duodenal effector mechanism for regulation of gastric emptying was noted.

As mentioned above, the sporadic contractions of phase II in the interdigestive state resemble the postprandial contractions and are manometrically difficult to distinguish by conventional time resolution of the recordings. Using high time resolution, allowing analysis of propagation of individual pressure waves, antegrade contractions were found to dominate in phase II in all four duodenal subsegments studied, (D1–D2) to (D4–D5). This was in contrast to the postprandial state where retrograde propagation of pressure waves was a prominent characteristic in the two proximal duodenal subsegments (D1–D2) and (D2–D3), but infrequent in the two distal subsegments (D3–D4) and (D4–D5) due to the pressure waves diverging in two different directions some 2–4 cm distal to pylorus. Thus, both in the interdigestive phase II and postprandially there are irregular contractions, but their different characteristics indicate varying functions. Furthermore, the origin of the retrograde pressure waves is predictable and seems to be a specific physiological phenomenon in certain situations.

Previous studies of postprandial duodenal motility have not revealed such a high frequency of retroperistalsis in the proximal duodenum as in our study. Kerrigan et al.6 found retrograde direction in only about 20% of all pressure waves in healthy controls. An explanation for this low frequency of retroperistalsis in the proximal duodenum, compared to our findings, could be the use of 3-cm intervals between recording points. With such a long distance between recording points1 the spatial resolution will be inadequate for analysis of the migration of individual pressure waves.7 For example, the interesting postprandial retroperistalsis in the immediate juxtapyloric area may be difficult to detect (cf. Figs 1 and 2). Thus, catheters with closely spaced recording points are a prerequisite for analysis of the migration of individual pressure waves.

The propulsive contractions of the distal stomach, tonic contractions of the proximal stomach and the pyloric activity are three well-known important mechanisms for the regulation of gastric emptying.15 Our observation of a high proportion of duodenal juxtapyloric retrograde contractions after a meal suggests a fourth important muscular mechanism for the regulation of gastric emptying. Our understanding of the regulation of gastric emptying is still incomplete. Further studies, taking this duodenal component into consideration, are warranted.

ACKNOWLEDGMENTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

We are indebted to Mrs Irmelin Hagman for excellent technical assistance. This study was supported by the Swedish Medical Research Council (No. 8288) and by the Faculty of Medicine, University of Göteborg.

References

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References
  • 1
    Keinke O, Schemann M, Ehrlein HJ. Mechanical factors regulating gastric emptying of viscous nutrient meals in dogs. Q J Exp Physiol 1984; 69: 78195.
  • 2
    Lin HC, Elashoff JD, Gu YG, Meyer JH. Nutrient feedback inhibition of gastric emptying plays a larger role than osmotically dependent duodenal resistance. Am J Physiol 1993; 265:G6726.
  • 3
    Miller J, Kauffman G, Elashoff J, Ohashi H, Carter D, Meyer JH. Search for resistances controlling gastric emptying of liquid meals. Am J Physiol 1981; 241:G40325.
  • 4
    Emeran A, Mayer EA.The physiology of gastric storage and emptying. In: Johnson LR ed. Physiology of the Gastrointestinal Tract, 3rd edn. New York: Raven Press, 1994:929–76.
  • 5
    Ahluwalia NK, Thompson DG, Barlow J, Heggie L. Human small intestinal contractions and aboral traction forces during fasting and after feeding. Gut 1994; 35: 62530.
  • 6
    Kerrigan DD, Read NW, Houghton LA, Taylor ME, Johnson AG. Disturbed gastroduodenal motility in patients with active and healed duodenal ulceration. Gastroenterology 1991; 100: 892900.
  • 7
    Björnsson ES, Abrahamsson H. Interdigestive gastroduodenal manometry in humans. Indication of duodenal phase III as a retroperistaltic pump. Acta Physiol Scand 1995; 153: 22130.
  • 8
    Castedal M, Björnsson E, Abrahamsson H. Duodenal juxtapyloric retroperistalsis in the interdigestive state. Scand J Gastroenterol 1997; 32: 797804.
  • 9
    Camilleri M. Perfused tube manometry. In: Kumar D, Wingate DW, eds. An Illustrated Guide to Gastrointestinal Motility, 2nd edn. Edinburgh: Churchill Livingstone, 1993:183–99.
  • 10
    Castedal M, Björnsson E, Gretarsdottir J, Fjälling M, Abrahamsson H. Duodenogastric reflux related to the migrating motor complex. Gastroenterology 1997; 112:A708 (abst.).
  • 11
    Lammers WJEP, Stephen B, Arafat K, Manefield GW. High resolution electrical mapping in the gastrointestinal system: initial results. Neurogastroenterol Mot 1996; 8: 20716.
  • 12
    Hausken T, Ödegaard S, Matre K, Berstad A. Antroduodenal motility and movements of luminal contents studied by duplex sonography. Gastroenterology 1992; 102: 158390.
  • 13
    Boulby P, Moore R, Gowland P, Spiller RC. Forward and backward antral flow during gastric emptying assessed by flow-sensitive magnetic resonance imaging (MRI): Effect of fat. Gastroenterology 1997; 112:A702(abst.).
  • 14
    Rao SSC, Lu C, Schulze-Delrieu K. Duodenum as an immediate brake to gastric outflow: a videofluoroscopic and manometric assessment. Gastroenterology 1996; 110: 7407.
  • 15
    Bueno L, Fioramonti J. Food and gastrointestinal motility. In: Kumar D, Wingate D eds. An Illustrated Guide to Gastrointestinal Motility, 2nd edn. Edinburgh: Churchill Livingstone, 1993: 130–43.